Vitamin D alters genes involved in follicular development and steroidogenesis in human cumulus granulosa cells

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 6, 2014, Pages

  Merhi, Zaher ^a   Doswell, Angela ^a   Krebs, Kendall ^a   Cipolla, Marilyn ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AROMATASE; CALCITRIOL; ESTRADIOL; FOLLITROPIN RECEPTOR; MESSENGER RNA; MUELLERIAN INHIBITING FACTOR; PROGESTERONE; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

3BETA HSD GENE; AMH GENE; AMHR II GENE; AROMATASE GENE; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; CUMULUS CELL; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN SYNTHESIS; FEMALE; FEMALE INFERTILITY; FERTILIZATION IN VITRO; FSH RECEPTOR GENE; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GRANULOSA CELL; HUMAN; HUMAN CELL; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE FLUID; PERICYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIOIMMUNOASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS;

3-HYDROXYSTEROID DEHYDROGENASES; AROMATASE; CALCITRIOL; CELLS, CULTURED; CUMULUS CELLS; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; FOLLICULAR FLUID; GENE EXPRESSION REGULATION; GONADAL STEROID HORMONES; HUMANS; OVARIAN FOLLICLE; RECEPTORS, PEPTIDE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

EID: 84902320560     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-4161     Document Type: Article

References (48)

1. Holick MF, Binkley NC, Bischoff-Ferrari HA, et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocr inol Metab. 2011; 96:1911-1930.
2. Ozkan S, Jindal S, Greenseid K, et al. Replete vitamin D stores predict reproductive success following in vitro fertilization. Fertil Steril. 2010;94:1314-1319.
3. Merhi Z, Seifer DB, Weedon J, et al. Circulating vitaminDcorrelates with serum antimullerian hormone levels in late-reproductive-aged women: Women's Interagency HIV Study. Fertil Steril. 2012;98: 228-234.
4. Halhali A, Acker GM, Garabedian M. 1,25-Dihydroxyvitamin D3 induces in vivo the decidualization of rat endometrial cells. J Reprod Fertil. 1991;91:59-64.
5. Twig G, Shina A, Amital H, Shoenfeld Y. Pathogenesis of infertility and recurrent pregnancy loss in thyroid autoimmunity. J Autoimmun. 2012;38:J275-J281.
6. Dicken CL, Isr ael DD, Davis JB, et al. Peripubertal vitamin D(3) deficiency delays puberty and disrupts the estrous cycle in adult female mice. Biol Reprod. 2012;87:51.
7. Luk J,Torrealday S,Neal Perry G Pal L Relevance of vitamin D in reproduction Hum Reprod. 2012 27 3015-3027.
8. Anifandis GM, Dafopoulos K, Messini CI, Chalvatzas N, Liakos N, Pournaras S, Messinis IE. Prog nostic value of follicular fluid 25-OH vitamin D and glucose levels in the IVF outcome. Reprod Biol Endocrinol. 2010;8:91.
9. Rudick B, Ingles S, Chung K, Stanczyk F, Paulson R, Bendikson K. Characterizing the influence of vitamin D levels on IVF outcomes. Hum Reprod. 2012;27:3321-3327.
10. Dennis NA, Houghton LA, Jones GT, van Rij AM, Morgan K, McLennan IS. The level o f serum anti-Mullerian hormone correlates with vitamin D status in men and women but not in boys. J Clin Endocrinol Metab. 2012;97:2450-2455.
11. Braga DP, Setti A, Figueira Rde C, Iaconelli A Jr., Borges E Jr. Seasonal variability in the fertilization rate of women undergoing assisted reproduction treatments. Gynecol Endocrinol. 2012;28:549-552.
12. Wood S, Quinn A, Troupe S, Kingsland C, Lewis-Jones I. Seasonal variation in assisted conception cycles and the influence of photoperiodism on outcome in in vitro fertilization cycles. Hum Fertil (Cambridge, England). 2006;9:223-229.
13. Pa rikh G, Varadinova M, Suwandhi P, et al. Vitamin D regulates steroidogenesis and insulin-like growth factor binding protein-1 (IGFBP-1) production in human ovarian cells. Horm Metab Res. 2010;42:754-757.
14. Davis J, Merhi Z, Berk TS, Neal-Perry G. Developmental Vitamin D3 deficiency differentially affects ovarian gene expression patterns in adult female mice. Fertil Steril. 2012;98(suppl 3);S32.
15. Durlinger AL, Gruijters MJ, Kramer P, et al. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology. 2002;143:1076-1084.
16. Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen AP, Hovatta O. Anti-Mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod. 2006;21:22 23-2227.
17. Campbell BK, Clinton M, Webb R. The role of anti-Mullerian hormone( AMH)during follicle development in a monovulatory species (sheep). Endocrinology. 2012;153:4533-4543.
18. Visser JA, Durlinger AL, Peters IJ, et al. Increased oocyte degeneration and follicular atresia during the estrous cycle in anti-Mullerian hormone null mice. Endocrinology. 2007;148:2301-2308.
19. Malloy PJ, Peng L, Wang J, Feldman D. Interaction of the vitamin D receptor with a vitamin D response element in the Mullerianinhibiting substance (MIS) promoter: regulation of MIS expression by calcitriol in prostate cancer cells. Endocrinology. 2009;150: 1580-1587.
20. Krishnan AV, Moreno J, Nonn L, et al. Novel pathways that contribute to the anti-proliferative and chemopreventive activities of calcitriol in prost ate cancer. J Steroid Biochem Mol Biol. 2007;103: 694-702.
21. Franks S. Controversy in clinical endocrinology: diagnosis of polycystic ovarian syndrome: in defense of the Rotterdam criteria. J Clin Endocrinol Metab. 2006;91:786-789.
22. Catteau-Jonard S, Jamin SP, Leclerc A, Gonzales J, Dewailly D, di Clemente N. Anti-Mullerian hormone, its receptor, FSH receptor, and androgen receptor gene s are overexpressed by granulosa cells from stimulated follicles in women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2008;93:4456-4461.
23. Merhi Z, Buyuk E, Berger DS, et al. Lepti n suppresses anti-Mullerian hormone gene expression through the JAK2/STAT3 pathway in luteinized granulosa cells of women undergoing IVF. Hum Reprod. 2013;28:1661-1669.
24. Jeppesen JV, Anderson RA, Kels ey TW, et al. Which follicles make the most anti-Mullerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod. 2013;19:519-527.
25. Liv ak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-C(T)] method. Methods. 2001;25:402-408.
26. Uyar A, Torrealday S, Seli E. Cumulus and granulosa cell markers of oocyte and embryo quality. Fertil Steril. 2013;99:979-997.
27. Borgbo T, Povlsen BB, Andersen CY, Borup R, Humaidan P, Grondahl ML. Comparison of gene exp ression profiles in granulosa and cumulus cells after ovulation induction with either human chorionic gonadotropin or a gonadotropin-releasing hormone agonist trigger. Fertil Steril. 2013;100:994-1001.
28. McAll ister JM, Mason JI, Byrd W, Trant JM, WatermanMR,Simpson ER. Proliferating human granulosa-lutein cells in long term monolayer culture: expression of aromatase, cholesterol side-chain cleavage, and 3-hydroxysteroid dehydrogenase. J Clin Endocrinol Metab. 1990;71:26-33.
29. Grossman MP,Nakajima ST,Fallat ME,Siow Y Mullerianinhibiting substance inhibits cytochrome P450 aromatase activity in human granulosa lutein cell cultu re Fertil Steril. 2008 89 1364-1370.
30. DutertreM,Gouedard L, Xavier F, LongWQ,di Clemente N, Picard JY, Rey R. Ovarian granulosa cell tumors express a functional membrane receptor for anti-Mullerian hormone in transgenic mice. Endocrinology. 200 1;142:4040-4046.
31. Zhan Y, Fujino A, MacLaughlin DT, et al. Mullerian inhibiting substance regulates its receptor/SMAD signaling and causes mesenchymal transition of the coelomic epithelial cells early in Mullerian duct regression. Development (Cambridge, England). 2006;133: 2359-2369.
32. Merhi Z, Messerlian GM, Minkoff H, et al. Comparison of serum and plasma measurements of Mullerian inhibiting substance. Fertil Steril. 2008;89:1836-1837.
33. Merhi Z, Minkoff H, Feldman J, Macura J, Rodriguez C, Seifer DB. Relationship of bariatric surgery to Mullerian-inhibiting substance l evels. Fertil Steril. 2008;90:221-224.
34. Devjak R, Fon Tacer K, Juvan P, Virant Klun I, Rozman D, Vrtacnik Bokal E. Cumulus cells gene expression profiling in terms of oocyte maturity i n controlled ovarian hyperstimulation using GnRH agonist or GnRH antagonist. PloS One. 2012;7:e47106.
35. Nilsson EE, Schindler R, Savenkova MI, Skinner MK. Inhibitory actions of anti-Mullerian hormone (AMH) on ovarian primordial follicle assembly. PloS One. 2011;6:e20087.
36. Baarends WM, Uilenbroek JT, Kramer P, et al. Anti-mullerian hormone and anti-mullerian hormone type II recepto r messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology. 1995;136:4951-4962.
37. American Society for Repro ductive Medicine. Testing and interpreting measures of ovarian reserve: a committee opinion. Fertil Steril. 2012;98:1407-1415.
38. Wojtusik J, Johnson PA. Vitamin D regulates anti-Mullerian hormone expression in granulosa cells of the hen. Biol Reprod. 2012; 86:91.
39. Aleyasin A, Hosseini MA, Mahdavi A, et al. Predictive value of the level of vitamin D in follicular fluid on the outcome of assiste d reproductive technology. Eur J Obstet Gynecol Reprod Biol. 2011; 159:132-137.
40. Macklon NS, Fauser BC. Follicle development during the normal menstrual cycle. Maturitas. 1998;30:181-188.
41. Son WY, Das M, Shalom-Paz E, Holzer H. Mechanisms of follicle selection and development. Minerva Ginecol. 2011;63:89-102.
42. Kawashima I, Okazaki T, Noma N, Nishibori M, Yamashita Y, Shimada M. Sequential exposure of porcine cumulus cells to FSH and/orLHis critical for appropriate expression of steroidogenic and ovulation-related genes that impact oocyte maturation in vivo and in vit ro. Reproduction. 2008;136:9-21.
43. Salhab M, Tosca L, Cabau C, et al. Kinetics of gene expression and signaling in bovine cumulus cells throughout IVM in different mediums in relation to oocyte developmental competence, cumulus apoptosis and progesterone secretion. Theriogenology. 2011;75: 90-104.
44. Yanase T, Mu YM, Nishi Y, et al. Regulation of aromatase by nuclear receptors. J Steroid Biochem Mol Biol. 2001;79:187-192.
45. Lundqvist J, Norlin M, Wikvall K. 1-,25-Dihydroxyvitamin D3 exerts tissue-specific effects on estrogen and androgen metabolism. Biochim Biophys Acta. 2011;1811:263-270.
46. Krishnan AV, Swami S, Feldman D. The potential therapeutic benefits of vitamin D in the treatment of estrogen receptor positive breast cancer. Steroids. 2012;77:1107-1112.
47. Krishnan AV, Swami S, Feldman D. Vitamin D and breast cancer: inhibition of estrogen synthesis and signaling. J Steroid Biochem Mol Biol. 2010;121:343-348.
48. Assou S, Haouzi D, De Vos J, Hamamah S. Human cumulus cells as biomarkers for embryo and pregnancy outcomes. Mol Hum Reprod. 2010;16:531-538.